Feeding height stratification in extant ecosystems
Ecological separation of coexisting species is achieved along the axes of food, time, and space [74, 75]. For example, the African savannah biome supports 31 species of large (> 5 kg), herbivorous mammals , and competition among its members is typically alleviated via the selection of different food types, the occupation of the same habitat at different times, or the occupation of different habitats at the same time [77–79]. The ecological separation of these ungulates may also be achieved along a vertical gradient, with different species feeding at different heights within the canopy or grass cover [77–83]. For example, Bell  demonstrated that, among grazers, zebra (Equus burchelli) tend to ingest the tallest, most fibrous portions of the herb layer, wildebeest (Connochaetes taurinus) and topi (Damaliscus korrigum) select the more nutritious middle layer, and Thomson’s gazelle (Gazella thomsoni) take in fruits from the ground. With the exception of the topi, this grazing succession is reflected by the decreasing body size of the animals (but see ). Similarly, feeding height stratification has been said to operate among browsing ungulates [77, 79, 81]. This hypothesis was tested explicitly on a subset of African browsers by du Toit , who found that giraffe (Giraffa camelopardalis), kudu (Tragelaphus strepsiceras), impala (Aepyceros melampus), and steenbok (Raphicerus campesteris) are stratified by mean feeding-height. On average, giraffe feed at heights between 2 and 3 m, kudu at heights near 1 m, and impala and steenbok at heights below 0.5 m. Although there was significant overlap between the browsing heights of some of these species, du Toit  observed that feeding height stratification is more pronounced during the dry season, when the use of woody browse is increased to compensate for the reduced availability of green forage in the herb layer. The long neck of the giraffe has been cited as an example of an adaptation to escape competition occurring at lower browsing heights .
Feeding height stratification in the Dinosaur Park Formation assemblage
As documented in extant taxa, numerous studies have commented on the importance of feeding height stratification as a mechanism for niche partitioning among herbivorous dinosaurs. For example, within the Upper Jurassic Morrison Formation of the western United States, up to five sauropod genera are thought to have lived in sympatry . Feeding height stratification has been repeatedly invoked as a means of facilitating their coexistence, with different sauropods using their long necks to feed at different heights within the environment. Evidence for this interpretation includes reconstructed neck morphology [33, 34, 56, 57], tooth wear analysis [44, 53–55, 58, 86], and jaw mechanics [52, 54].
Feeding height stratification has likewise been invoked to account for the diverse herbivorous dinosaur fauna of the DPF [12, 13, 33], but no formal test of this hypothesis has been conducted to date. Notably, most treatments of feeding height stratification make little or no mention of the small ornithischians that inhabited the Late Cretaceous landscape of Laramidia. This is probably because these forms are both poorly known and relatively rare in the fossil record. However, Brown et al.  recently demonstrated a substantial taphonomic size bias in the record of the DPF, and it is therefore likely that small ornithischians comprised a larger proportion of the herbivore fauna than previously assumed. The MFHs of these animals were probably restricted to less than approximately 1 m, which may have placed them in competition with the megaherbivores discussed below.
Béland and Russell  and Coe et al.  suggested that ankylosaurs from the DPF exhibited different MFHs, with Euoplocephalus feeding on herbs below 0.5 m and Panoplosaurus feeding on woody vegetation up to 1 m. However, the current data do not support this hypothesis. The mean MFH of Euoplocephalus is closer to 0.8 m, whereas that of Panoplosaurus approximates 0.9 m. There is also considerable overlap of MFH between these taxa, with some specimens of Euoplocephalus reaching as high as 0.88 m, and some specimens of Panoplosaurus only reaching 0.77 m. Apart from the reduced ankylosaur sample (see below), this moderate overlap of MFHs likely accounts for the fact that Euoplocephalus and Panoplosaurus do not differ significantly from one another. The contention of Weishampel and Norman  that ankylosaurs were generally restricted to browsing between 1 and 2 m is not supported here. By extending the forelimb proportions of Euoplocephalus (AMNH 5403) to the 542 mm-long humerus of Ankylosaurus (AMNH 5214), the largest known ankylosaur, the total forelimb length is estimated to be only 1.1 m.
Several authors [12, 13, 87, 88] have likewise suggested that ceratopsids were capable of reaching heights of 2 m; however, no evidence was provided for this value. Instead, our results indicate that ceratopsids more likely browsed no higher than approximately 1 m, as suggested by Dodson . One well-preserved specimen of Triceratops (NSM PV 20379), among the largest ceratopsids that ever existed, could not reach above 1.2 m, either .
The common claim that hadrosaurids could reach heights up to 4 m [7, 12, 13, 33, 87, 88] is supported by our results. The largest hadrosaurids from the DPF, Gryposaurus and Prosaurolophus, probably could reach heights approaching 5 m in a bipedal posture (Figure 3). Despite these maxima, some authors [87, 89] have proposed that hadrosaurid feeding was probably concentrated below 2 m, which would accord with the quadrupedal feeding postures calculated here.
Both vertebrate microfossil and skeletal remains suggest that hadrosaurids formed approximately 40% of the herbivorous dinosaur assemblage in the DPF ecosystem [7, 61], which likely translates to a greater proportion of the herbivore biomass because hadrosaurids are the largest members of the fauna. The remainder of herbivores, notably the large ceratopsids and ankylosaurs which combined form approximately an equivalent proportion in terms of relative abundance, fed at or below the 1 m mark. Although feeding heights could not be discriminated below 1 m, the fact that hadrosaurids could reach up to 5 m and were therefore segregated from all other herbivores is likely fundamental in partitioning the resource base. Importantly, hadrosaurids were capable of reaching shrubs and low-growing trees that were beyond the reach of ceratopsids, ankylosaurs, and other small herbivores, effectively dividing the herbivores in terms of relative abundance. This may also have allowed hadrosaurids to escape resource stresses imparted by low browsers, and may have facilitated the co-existence of large herds of ceratopsids and highly abundant hadrosaurids [20, 90] in DPF palaeoecosystems.
Dinosaur browsing and vegetation structure
The prevailing climate of the DPF has been described as warm temperate, as revealed by tree-, tooth-, and bone-growth ring data [91, 92], sedimentological data , and biogeographic data [94, 95]. Regional leaf physiognomic data have also reinforced this interpretation . This climate is, in part, thought to have given rise to both open and closed habitats [96–99] akin to those of modern ecosystems . Braman and Koppelhus (:124) describe the landscape of the DPF as having been “wet everywhere, at least for portions of the year”, with dense vegetation lining the rivers, and more open habitats occurring further distally.
The open habitats of the DPF and surrounding regions were likely dominated by ferns and low-growing angiosperms. Coe et al. (: 235) even proposed the existence of extensive “fern prairies”, analogous to modern grasslands, but Tiffney  stressed that evidence for such fern-dominated communities is lacking. Nonetheless, Wing et al.  subsequently reported one exceptional fossil flora from the mid-Maastrichtian in which ferns and other “pteridophytes” account for nearly 50% of the total ground cover. By comparison, these same plants account for approximately 40% of the total palynomorph abundance in the DPF .
The Late Cretaceous saw the radiation of the angiosperms, which typically took the form of “weedy” herbs and shrubs growing in open or marginal habitats [12, 33, 97, 98, 101, 104, 105]. Angiosperm trees, although inferred to have existed elsewhere , probably did not occur in the DPF, as evidenced by the lack of diagnostic fossil wood . It is commonly argued (:125[104, 106]) that angiosperms occurred most regularly in coastal and fluvial depositional settings, occupying “stream-side and aquatic habitats, the forest understory and early successional thickets”; however, Wheeler and Lehman  noted the existence of angiosperm-dominated communities in southern upland environments as well, where conifers were otherwise thought to have dominated [98, 104]. By virtue of their r-selected life history strategies, it is likely that angiosperms were capable of growing in a wide variety of habitats .
A common theme in the literature is the persistence of open-habitat cycadophytes (bennettitaleans and cycads) as forage for Late Cretaceous herbivores [34, 97, 108–113]. However, bennettitaleans went extinct by the Santonian , and cycads were probably absent from the DPF ([65, 115, 116], D. R. Braman, pers. comm., 2012), having been replaced by angiosperms [98, 117]. It is by no means clear that cycadophytes were common enough elsewhere during the Late Cretaceous to support dense megaherbivore populations, but their seed coats may have served to supplement dinosaur diets [97, 109–111].
Unlike tropical forests, temperate forests typically exhibit limited stratification , and there is little reason to suspect that the temperate forests of the DPF were any different. Wolfe and Upchurch  proposed that such forests were, in fact, relatively sparse, with sunlight often penetrating fully through to the ground. Palynofloral and macroplant evidence from the DPF suggests that the forest canopy was formed primarily by taxodiaceous, cupressaceous, and podocarpaceous conifers [100, 119, 120], a composition typical of most Late Cretaceous warm temperate forests . Angiosperm shrubs may  or may not ) have formed an understory, alongside tree ferns and gymnosperm saplings . The herb layer would have included ferns, lycopods, angiosperm herbs, and gymnosperm saplings, and ground cover comprised mosses, lichens, fungi, hornworts, and decaying vegetable matter .
Opinions vary about the degree to which habitat structure influenced the regional distribution of the Late Cretaceous herbivorous dinosaurs. Some [97, 101, 112] argued that the megaherbivorous forms were likely restricted to feeding in open habitats, partly as a result of their large sizes. However, it appears that the forests of the Late Cretaceous were not particularly dense , and probably did not inhibit the movement of even the more massive herbivores [13, 96]. Alternatively, Baszio  suggested that, within the DPF, ankylosaurs and ceratopsids occupied open habitats, whereas hadrosaurids lived in forested environments. His reasoning was that ankylosaurs and ceratopsids, being limited in their range of vertical movements, could not have taken full advantage of stratified forest vegetation in the same way that hadrosaurids presumably could. However, it is unlikely that hadrosaurids could have accessed the entire forest structure; the canopy was almost certainly out of reach, particularly if Late Cretaceous taxodiaceous and cupressaceous conifers grew as tall as their modern descendants (> 90 m). Hadrosaurids likely could forage among the shrubs of the forest understory, but shrubs were abundant in more open habitats as well [12, 33, 97, 98, 101, 105]. In that case, there is little reason to suspect that hadrosaurids could not have occupied both open and closed habitats , alongside ankylosaurs and ceratopsids.
This does not contradict the idea that certain groups may have preferred certain environments over others. Various lines of sedimentological evidence have been brought to bear on the matter [7, 12, 60, 61, 91, 123, 124]. There simply does not appear to have been any major structural obstacles to impede the movement of these animals. Consider that elephants, which are comparable in size to the megaherbivorous dinosaurs considered here, regularly occupy even dense forests and thickets in search of food . In fact, their movements and feeding habits typically result in the creation of new, more navigable habitats [126, 127].
Regardless of where hadrosaurids spent most of their time, it is likely that they usually foraged quadrupedally on abundant, low-lying herbage [87, 89, 128], occasionally rearing up onto their hindlimbs to feed among the angiosperm shrubs. Additional evidence for bipedal feeding in these animals comes from the Campanian aged Blackhawk Formation of Utah, where hundreds of dinosaur footprints are preserved in association with taxodiaceous conifer and palm roots and fallen logs . In many places, pes prints attributed to hadrosaurids are found straddling the roots. The fact that manus prints are not also found in these areas suggests that these animals were rearing up to feed on the high foliage. This bipedal feeding behaviour would have been particularly beneficial in instances where large herds of low-browsing ceratopsids were passing through the same area [17, 20–22]. Dietary niche partitioning could have been achieved among hadrosaurids if they utilized different levels within the shrub layer, as do living ruminants . This may also have served to limit niche overlap between different ontogenetic stages of the same species . The larger feeding heights of the hadrosaurids suggest that these animals were able to reach a wider variety of plant types than other sympatric herbivores. Circumstantial evidence for diet in these animals comes from multiple examples of fossil gut contents [131–133], which preserve conifer and angiosperm browse, including twigs and stems, bark, seeds, leaves, and fruit. Probable hadrosaurid coprolites [134, 135] also contain abundant fungally-degraded conifer wood, which would presumably indicate that hadrosaurids fed at ground level at least occasionally. However, in light of the problems associated with the attribution of some of these fossils [32, 132, 136, 137], their interpretation as dietary residues must be regarded with due caution.
Ankylosaurs, ceratopsids, and small ornithischians may have partitioned the herb layer by feeding height, as do the ungulates of the Serengeti today . Ceratopsids, being slightly taller, may have even facilitated the existence of the other forms by cropping the herb layer to expose new growth. Of course, this is a highly speculative scenario requiring further investigation. Unfortunately, no ceratopsid gut contents are known by which to gauge these ideas, but an ankylosaurid cololite from Australia is reported to contain fibrous tissue (probably leaves), angiosperm fruits or endocarps, small seeds, and possible fern sporangia . Ankylosaurs, it would seem, consumed less woody browse than hadrosaurids, which is in line with the interpretation given here.
One final aspect of herbivorous dinosaur ecology bears consideration. Elephants are known to regularly fell trees up to 10 m tall to feed on the otherwise unreachable browse, effectively increasing the feeding envelope of these animals up to three times [13, 125]. It is possible that the megaherbivores of the DPF were capable of the same behaviour [13, 65]. If so, tree felling may have served to increase dietary overlap between these animals, with the squat ankylosaurs and ceratopsids consuming foliage otherwise in reach of hadrosaurids alone. Unfortunately, while tree felling behaviour among dinosaurs is plausible, there is not yet any evidence supporting this speculation. Similarly, scenarios involving hypsilophodontids and pachycephalosaurids climbing trees to increase their feeding heights , while not impossible, are implausible owing to a lack of appropriate skeletal adaptation [139, 140]. For these reasons, such highly speculative behaviours are not considered further.
Evolutionary palaeoecological implications
There is no convincing evidence that feeding height stratification, as revealed by reconstructed MFH, played as significant a role in facilitating herbivorous dinosaur niche partitioning in the DPF as previously assumed [12, 13]. Despite the 18 genera considered here—six or more of which typically coexisted at a time —only four statistically distinct MFHs are detected. If niche partitioning did allow herbivorous dinosaurs from the DPF to coexist, it may have been achieved by other means in addition to feeding height stratification. Although this hypothesis has yet to be subjected to rigorous testing, multiple morphological features have been proposed to have fostered the coexistence of these herbivores. For example, Carpenter [38–41] suggested that differences between the tooth and beak shapes of ankylosaurids and nodosaurids may have allowed these taxa to specialize on different plant types. Similarly, differences between centrosaurines and chasmosaurines in cranial , mandibular , and beak [8, 43] morphology have been cited as evidence for dietary niche partitioning. Finally, variations in beak shape [7, 34, 36, 44], tooth morphology [36, 46], and skeletal proportions  are thought to have enabled hadrosaurines and lambeosaurines to forage differentially. Many of these assumptions have not been tested and require further examination, particularly in light of questions regarding the significance of intraspecific variation and the influence of time-averaging.
The disappearance of ankylosaurs from the upper intervals of MAZ-2 of the DPF  suggests the possibility that some change in their habitat structure caused their displacement. Although it is by no means obvious whether such a change did occur, the gradual transgression of the Western Interior Seaway over the approximately 1.5 Ma span of the DPF undoubtedly would have had some influence on the palaeoflora. It may be that some of the herbaceous plants preferred by the ankylosaurs disappeared, but this scenario is difficult to test at present.
Overall, the distribution of herbivore MFHs changed minimally over the course of the DPF. Rather, MFHs were quite stable in spite of rapid and continual species turnover, and roughly the same ratio of low to high browsers was upheld (Figure 3B,C). This, in turn, suggests that time-averaging does not completely obscure palaeoecological signals within the DPF, other than to artificially inflate estimates of standing crop biodiversity. It also suggests that the MFHs maintained by their respective species were evolutionarily stable strategies, and may reflect correlated stability in the growth habits of the surrounding plants. Major changes in habitat structure do not appear to have occurred until the beginning of the Paleocene [101, 105], underscoring the importance of low-growing herbage in sustaining Late Cretaceous herbivore faunas.
Finally, it must be noted that, while differences in estimated MFHs are consistent with the hypothesis of feeding height stratification, they are not sufficient for this hypothesis to be true. It is possible that, despite these differences, all herbivore taxa from the DPF spent most of their time feeding at ground level [33, 34]. In this sense, they may be compared to grazing ungulates, which spend most of their time feeding on low grasses, despite being physically capable of reaching higher browse. Therefore, although it seems likely from an ecological perspective that the herbivorous dinosaur fauna of the DPF exhibited some form of feeding height stratification, competing hypotheses about the role of this mechanism in the facilitation of niche partitioning are underdetermined  by the available evidence. To reject the null hypothesis of no feeding height stratification, it would be necessary to show that the herbivorous dinosaurs browsed to their full potential, utilizing their entire reconstructed MFHs, and did not simply spend all their time feeding at ground level. Unfortunately, this type of behaviour simply does not fossilize. Nevertheless, it may be possible to approximate the amount of time spent feeding at different heights by observing other aspects of morphology. For example, it has been shown that low-level grazers often possess a suite of cranial characteristics that allow them to efficiently crop short grass, including wide, ventrally deflected muzzles, elongate faces, transversely wide paroccipital processes, deep mandibles, and tall withers [142–150]. Similarly, primates feeding close to the ground generally possess narrower dental microwear scratches than those feeding higher up in the forest canopy, a function of mean particle size and the ratio of soil particles to phytoliths [151–153]. These same features might be sought among the herbivorous dinosaurs to more accurately determine their browsing habits.